[en] The levels of eighteen trace elements (TEs) were evaluated in association with stable isotopes (δ15N, δ34S, and δ13C) in feathers and eggs of five migratory species breeding on the Antarctic Peninsula to test the factors that influence their exposure to contaminants. The feathers of seabirds migrating to the Northern Hemisphere (South polar skua) have concentrations (mean ± SD, μg. g-1) of Li (1.71 ± 2.08) and Mg (1169.5 ± 366.8) one order of magnitude higher than southern migrants, such as Snowy sheathbill Li (0.01 ± 0.005) and Mg (499.6 ± 111.9). Feathers had significantly higher concentrations for 11 of a total of 18 metals measured compared to eggs. South polar skua have higher concentrations of all TEs in eggs compared to antarctic tern. Therefore, the present study showed that migration and trophic ecology (δ15N, δ13C, and δ34S) influence Fe, Mn, Cu, and Se concentrations in feathers of Antarctic seabirds. The concentrations of Cu, Mn, Rb, Zn, Pb, Cd, Cr are higher than previously reported, which may be due to increased local and global human activities.
Padilha, J A; Biophysics Institute, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil, CBMA - Centre for Molecular and Environmental Biology/ARNET-Aquatic Research Network & IB-S, Institute of Science and Innovation for Bio-Sustainability, Department of Biology, University of Minho, Campus Gualtar, 4710-057 Braga, Portugal. Electronic address: janeide.padilha@ufrj.br
Carvalho, G O; Biophysics Institute, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Espejo, W; Department of Soils and Natural Resources, Facultad de Agronomía, Universidad de Concepción, P.O. Box 537, Chillán, Chile
Pessôa, A R L; Biophysics Institute, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Cunha, L S T; Biophysics Institute, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Costa, E S; Mestrado Profissional em Ambiente e Sustentabilidade, Universidade Estadual do Rio Grande do Sul, Rua Assis Brasil, 842, Centro, São Francisco de Paula, Rio Grande do Sul, Brazil
Torres, J P M; Biophysics Institute, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution
Das, Krishna ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Dorneles, Paulo Renato ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Language :
English
Title :
Trace elements in migratory species arriving to Antarctica according to their migration range
This work was supported by the Brazilian National Council for Scientific and Technological Development (CNPq) through CNPq / MCT 557049 / 2009 - 1, as well as through a Universal Call CNPq - Project from PRD (proc. 432518 / 2016 - 9). This work was also supported by a scientific cooperation established between the Brazilian Foundation for the Coordination and Improvement of Higher Level or Education Personnel (CAPES - process numbers 88881.154725 / 2017 - 01 88887.154724 / 2017-00) and Wallonie Bruxelles International (WBI, from Belgium), coordinated by PRD and KD, as well as by the Rio de Janeiro State Government Research Agency [FAPERJ - E-26 / 111.505 / 2010 and E - 26 / 210.464 / 2019 (249593)]. Thanks for C. Delforge for technical assistance during chemical analyses. We would like to thank the Brazilian Navy, which provided logistical support in Antarctica through the “Secretariat of the Interministerial Commission for the Resources of the Sea” (SECIRM). GL and KD are Senior F.R.S.- FNRS research associate. PRD has a research grant from CNPq (PQ-2 proc. 08733 / 2019 - 3). WE is supported by the FONDECYT 3200302 of the Agencia Nacional de Investigación y Desarrollo de Chile (ANID). GOC received a doctoral scholarship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq- proc. 141460/2020-2), Ministério da Ciência, Tecnologia e Inovação.Professor Das was responsible for funding acquisition, administration, and supervision of the project (CAPES - process numbers 88,881.154725/2017–0188887.154724/2017–00) and Wallonie Bruxelles International (WBI, from Belgium) that allowed the analysis of trace elements and stable isotopes at the University of Liége. She contributed to the conceptualization, writing, and review of the paper.This work was supported by the Brazilian National Council for Scientific and Technological Development (CNPq) through CNPq / MCT 557049 / 2009 - 1 , as well as through a Universal Call CNPq - Project from PRD (proc. 432518 / 2016 - 9 ). This work was also supported by a scientific cooperation established between the Brazilian Foundation for the Coordination and Improvement of Higher Level or Education Personnel (CAPES - process numbers 88881.154725 / 2017 - 01 88887.154724 / 2017-00 ) and Wallonie Bruxelles International (WBI, from Belgium), coordinated by PRD and KD, as well as by the Rio de Janeiro State Government Research Agency [FAPERJ - E-26 / 111.505 / 2010 and E - 26 / 210.464 / 2019 (249593) ]. Thanks for C. Delforge for technical assistance during chemical analyses. We would like to thank the Brazilian Navy, which provided logistical support in Antarctica through the “Secretariat of the Interministerial Commission for the Resources of the Sea” (SECIRM). GL and KD are Senior F.R.S.- FNRS research associate. PRD has a research grant from CNPq (PQ-2 proc. 08733 / 2019 - 3 ). WE is supported by the FONDECYT 3200302 of the Agencia Nacional de Investigación y Desarrollo de Chile (ANID). GOC received a doctoral scholarship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq- proc. 141460/2020-2), Ministério da Ciência, Tecnologia e Inovação.
Anderson, O.R.J., Phillips, R.A., Shore, R.F., McGill, R.A.R., McDonald, R.A., Bearhop, S., Element patterns in albatrosses and petrels: influence of trophic position, foraging range, and prey type. Environ. Pollut. 158 (2010), 98–107, 10.1016/j.envpol.2009.07.040.
Ashbaugh, H.M., Conway, W.C., Haukos, D.A., Collins, D.P., Comer, C.E., French, A.D., Evidence for exposure to selenium by breeding interior snowy plovers (Charadrius nivosus) in saline systems of the Southern Great Plains. Ecotoxicology 27 (2018), 703–718, 10.1007/s10646-018-1952-2.
Bargagli, R., Environmental contamination in Antarctic ecosystems. Sci. Total Environ. 400 (2008), 212–226, 10.1016/j.scitotenv.2008.06.062.
Bighetti, G.P., Padilha, J.A., Cunha, L.S.T., Kasper, D., Malm, O., Mancini, P.L., Bioaccumulation of mercury is equal between sexes but different by age in seabird (Sula leucogaster) population from southeast coast of Brazil. Environ. Pollut., 285, 2021, 117222, 10.1016/j.envpol.2021.117222.
Borghello, P., Torres, D.S., Montalti, D., Ibañez, A.E., Diet of the Brown Skua (Stercorarius antarcticus lonnbergi) at Hope Bay, Antarctic Peninsula: differences between breeders and non-breeders. Polar Biol. 42 (2019), 385–394, 10.1007/s00300-018-2429-8.
Burger, J., Metals in avian feathers: bioindicators of environmental pollution. Rev. Environ. Toxicol. 5 (1993), 203–311.
Burger, J., Gochfeld, M., Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. Sci. Total Environ. 257 (2000), 37–52, 10.1016/S0048-9697(00)00496-4.
Burger, J., Gochfeld, M., Metals in albatross feathers from midway atoll: influence of species, age, and nest location. Environ. Res. 82 (2000), 207–221, 10.1006/enrs.1999.4015.
Burger, J., Gochfeld, M., Spatial and temporal patterns in metal levels in eggs of common terns (Sterna hirundo) in New Jersey. Sci. Total Environ. 311 (2003), 91–100, 10.1016/S0048-9697(03)00135-9.
Calizza, E., Signa, G., Rossi, L., Vizzini, S., Careddu, G., Tramati, C.D., Caputi, S.S., Mazzola, A., Costantini, M.L., Trace elements and stable isotopes in penguin chicks and eggs: a baseline for monitoring the Ross Sea MPA and trophic transfer studies. Mar. Pollut. Bull., 170, 2021, 112667, 10.1016/j.marpolbul.2021.112667.
Carravieri, A., Bustamante, P., Labadie, P., Budzinski, H., Chastel, O., Cherel, Y., Trace elements and persistent organic pollutants in chicks of 13 seabird species from Antarctica to the subtropics. Environ. Int., 134, 2020, 105225, 10.1016/j.envint.2019.105225.
Casaux, R., Baroni, A., Ramón, A., Favero, M., Silva, P., Aspects of the foraging behaviour of the Antarctic Tern Sterna vittatagaini at Harmony Point, South Shetland Islands. Polar Biol. 31 (2008), 327–331, 10.1007/s00300-007-0362-3.
Castro, M.F., Neves, J.C.L., Francelino, M.R., Schaefer, C.E.G.R., Oliveira, T.S., Seabirds enrich Antarctic soil with trace metals in organic fractions. Sci. Total Environ., 785, 2021, 147271, 10.1016/j.scitotenv.2021.147271.
Celis, J.E., Barra, R., Espejo, W., González-Acuña, D., Jara, S., Trace element concentrations in biotic matrices of gentoo penguins (Pygoscelis papua) and coastal soils from different locations of the Antarctic Peninsula. Water Air Soil Pollut., 226, 2014, 2266, 10.1007/s11270-014-2266-5.
Celis, J.E., Barra, R., Chiang, G., González-Acuña, D., Espejo, W., Studying heavy metals on Antarctica by using non invasive biotic samples of penguins. Oceanogr.Fish.Open Access J. 7 (2018), 23–24.
Cipro, C.V.Z., Bustamante, P., Petry, M.V., Montone, R.C., Seabird colonies as relevant sources of pollutants in Antarctic ecosystems: part 1 - trace elements. Chemosphere 204 (2018), 535–547, 10.1016/j.chemosphere.2018.02.048.
Coplen, T.B., Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun. Mass Spectrom. 25 (2011), 2538–2560, 10.1002/rcm.5129.
De Moreno, J.E.A., Gerpe, M.S., Moreno, V.J., Vodopivez, C., Heavy metals in Antarctic organisms. Polar Biol. 17 (1997), 131–140.
Drouillard, K.G., Norstrom, R.J., Quantifying maternal and dietary sources of 2,2′,4,4′,5,5′-hexachlorobiphenyl deposited in eggs of the ring dove (Streptopelia risoria). Environ. Toxicol. Chem. 20 (2001), 561–567, 10.1002/etc.5620200315.
Einoder, L.D., MacLeod, C.K., Coughanowr, C., Metal and isotope analysis of bird feathers in a contaminated estuary reveals bioaccumulation, biomagnification, and potential toxic effects. Arch. Environ. Contam. Toxicol. 75 (2018), 96–110, 10.1007/s00244-018-0532-z.
Espejo, W., Sandoval, M., Celis, J.E., López, J., Riquelme, F., POSIBLES IMPLICANCIAS AMBIENTALES DEBIDO A LA RESISTENCIA A METALES PESADOS EN BACTERIAS AISLADAS DE EXCRETAS DEL PINGÜINO DE HUMBOLDT. Interciencia 42 (2017), 324–330.
Espejo, W., Celis, J.E., GonzÃlez-Acuña, D., Banegas, A., Barra, R., Chiang, G., A global overview of exposure levels and biological effects of trace elements in penguins. de Voogt, P., (eds.) Reviews of Environmental Contamination And Toxicology Reviews of Environmental Contamination And Toxicology, Vol. 245, 2018, Springer International Publishing, Cham, 1–64, 10.1007/398_2017_5.
Espejo, W., Padilha, J.de A., Kidd, K.A., Dorneles, P., Malm, O., Chiang, G., Celis, J.E., Concentration and trophic transfer of copper, selenium, and zinc in marine species of the Chilean Patagonia and the Antarctic Peninsula Area. Biol. Trace Elem. Res. 197 (2020), 285–293, 10.1007/s12011-019-01992-0.
Jaspers, V.L.B., Covaci, A., Herzke, D., Eulaers, I., Eens, M., Bird feathers as a biomonitor for environmental pollutants: prospects and pitfalls. TrAC Trends Anal. Chem. 118 (2019), 223–226, 10.1016/j.trac.2019.05.019.
Jerez, S., Motas, M., Benzal, J., Diaz, J., Vidal, V., D'Amico, V., Barbosa, A., Distribution of metals and trace elements in adult and juvenile penguins from the Antarctic Peninsula area. Environ. Sci. Pollut. Res. 20 (2013), 3300–3311, 10.1007/s11356-012-1235-z.
Jerez, S., Motas, M., Palacios, M.J., Valera, F., Cuervo, J.J., Barbosa, A., Concentration of trace elements in feathers of three Antarctic penguins: geographical and interspecific differences. Environmental Pollution, Nitrogen Deposition, Critical Loads And Biodiversity, 159, 2011, 2412–2419, 10.1016/j.envpol.2011.06.036.
Kopp, M., Peter, H.-U., Mustafa, O., Lisovski, S., Ritz, M.S., Phillips, R.A., Hahn, S., South polar skuas from a single breeding population overwinter in different oceans though show similar migration patterns. Mar. Ecol. Prog. Ser. 435 (2011), 263–267, 10.3354/meps09229.
Lehnert, K., Ronnenberg, K., Weijs, L., Covaci, A., Das, K., Hellwig, V., Siebert, U., Xenobiotic and immune-relevant molecular biomarkers in harbor seals as proxies for pollutant burden and effects. Arch. Environ. Contam. Toxicol. 70 (2016), 106–120, 10.1007/s00244-015-0202-3.
Mallory, M.L., Mahon, L., Tomlik, M.D., White, C., Milton, G.R., Spooner, I., Colonial marine birds influence island soil chemistry through biotransport of trace elements. Water Air Soil Pollut., 226, 2015, 31, 10.1007/s11270-015-2314-9.
Marques, R.C., Garrofe Dórea, J., Rodrigues Bastos, W., de Freitas Rebelo, M., de Freitas Fonseca, M., Malm, O., Maternal mercury exposure and neuro-motor development in breastfed infants from Porto Velho (Amazon), Brazil. Int. J. Hyg. Environ. Health 210 (2007), 51–60, 10.1016/j.ijheh.2006.08.001.
Metcheva, R., Yurukova, L., Teodorova, S., Nikolova, E., The penguin feathers as bioindicator of Antarctica environmental state. Sci. Total Environ. 362 (2006), 259–265, 10.1016/j.scitotenv.2005.05.008.
Metcheva, R., Yurukova, L., Teodorova, S.E., Biogenic and toxic elements in feathers, eggs, and excreta of Gentoo penguin (Pygoscelis papua ellsworthii) in the Antarctic. Environ. Monit. Assess. 182 (2011), 571–585, 10.1007/s10661-011-1898-9.
Nordberg, G.F., Fowler, B.A., Nordberg, M., Handbook on the Toxicology of Metals. 2014, Academic Press.
Nygård, T., Lie, E., Røv, N., Steinnes, E., Metal dynamics in an Antarctic food chain. Mar. Pollut. Bull. 42 (2001), 598–602, 10.1016/S0025-326X(00)00206-X.
Ohlendorf, H., Heinz, G., Selenium in Birds. 2011, USGS Staff – Published Research.
Padilha, J.D.A., Da Cunha, L.S.T., De Castro, R.M., Malm, O., Dorneles, P.R., Exposure of magnificent frigatebird (Fregata magnificens) and brown booby (Sula leucogaster) to metals and selenium in Rio de Janeiro State (Brazil) coastal waters. Orbital: Electron. J. Chem. 10 (2018), 254–261, 10.17807/orbital.v10i2.1050.
Padilha, J.A., Carvalho, G.O., Espejo, W., Souza, J.S., Pizzochero, A.C., Cunha, L.S.T., Costa, E.S., Pessôa, A.R.L., Almeida, A.P., Torres, J.P.M., Lepoint, G., Michel, L.N., Das, K., Dorneles, P.R., Factors that influence trace element levels in blood and feathers of Pygoscelis penguins from South Shetland Islands,Antarctica. Environ. Pollut., 284, 2021, 117209, 10.1016/j.envpol.2021.117209.
Patterson, D.L., Hunter, S., Giant Petrel Macronectes spp. band recovery analysis from the International Giant Petrel Banding Project, 1988/89. Mar. Ornithol. 28 (2000), 69–74.
R Core Team. R: A language and environment for statistical computing [Computer software], 2019, R Foundation for Statistical Computing.
Roscales, J.L., González-Solís, J., Zango, L., Ryan, P.G., Jiménez, B., Latitudinal exposure to DDTs, HCB, PCBs, PBDEs and DP in giant petrels (Macronectes spp.) across the Southern Ocean. Environ. Res. 148 (2016), 285–294, 10.1016/j.envres.2016.04.005.
Roscales, J.L., Vicente, A., Ryan, P.G., González-Solís, J., Jiménez, B., Spatial and interspecies heterogeneity in concentrations of perfluoroalkyl substances (PFASs) in seabirds of the Southern Ocean. Environ. Sci. Technol. 53 (2019), 9855–9865, 10.1021/acs.est.9b02677.
Rückamp, M., Braun, M., Suckro, S., Blindow, N., Observed glacial changes on the King George Island ice cap, Antarctica, in the last decade. Glob. Planet. Chang. 79 (2011), 99–109, 10.1016/j.gloplacha.2011.06.009.
Santamans, A.C., Boluda, R., Picazo, A., Gil, C., Ramos-Miras, J., Tejedo, P., Pertierra, L.R., Benayas, J., Camacho, A., Soil features in rookeries of Antarctic penguins reveal sea to land biotransport of chemical pollutants. PLOS ONE, 12, 2017, e0181901, 10.1371/journal.pone.0181901.
Santos, I.R., Silva-Filho, E.V., Schaefer, C., Maria Sella, S., Silva, C.A., Gomes, V., Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ. Pollut. 140 (2006), 304–311, 10.1016/j.envpol.2005.07.007.
Sick, H., Haffer, J., Alvarenga, H.F., Pacheco, J.F., Barruel, P., Ornitologia Brasileira. 1997, Nova Fronteira, Rio de Janeiro.
Souza, J.S., Kasper, D., da Cunha, L.S.T., Soares, T.A., de Lira Pessoa, A.R., de Carvalho, G.O., Costa, E.S., Niedzielski, P., Torres, J.P.M., Biological factors affecting total mercury and methylmercury levels in Antarctic penguins. Chemosphere, 261, 2020, 127713, 10.1016/j.chemosphere.2020.127713.
Wang, W.-X., Bioaccumulation and biomonitoring. Marine Ecotoxicology, 2016, Elsevier, 99–119.
Wing, S.R., Wing, L.C., O'Connell-Milne, S.A., Barr, D., Stokes, D., Genovese, S., Leichter, J.J., Penguins and seals transport limiting nutrients between offshore pelagic and coastal regions of Antarctica under changing sea ice. Ecosystems, 2020, 10.1007/s10021-020-00578-5.
